Uncovering lineage-specific evolutionary innovations in Actinopterygii by deciphering synteny profiles among a hundred genomes

Abstract Gene order is non-random in eukaryotes and significantly affected by whole-genome duplication (WGD). Although WGDs are a well-documented factor in the evolution of ray-finned fish (Actinopterygii), no large-scale phylogenomic synteny profiling for these species is currently available. Here, we constructed a comprehensive phylogenomic synteny profile for Actinopterygii using one hundred high-quality genomes. The resulting profile revealed extensive conserved and lineage-specific microsynteny clusters across major ray-finned fish lineages. Several synteny-conserved single-copy genes in diploids were consistently retained as duplicates in polyploids, a phenomenon observed irrespective of the timing of WGDs, e.g., casc3, upf2, upf3a, and upf3b, which are crucial in exon-exon junction complex-dependent nonsense-mediated mRNA decay and likely play pivotal roles in the degeneration of thousands of duplicates post-WGD. Lineage-specific microsynteny clusters also highlight candidate genes associated with important lineage-specific traits, including vdra, gnal2, ptpra, and cep83 in ostariophysians associated with the Weberian apparatus and pheromone-elicited fright reactions, immunity-related genes associated with longevity in Acipenseriformes, duplicated klhl10 and cfap45 in cichlid spermatogenesis, and duplicated tyr-like genes in salmonid black-spot pigmentation. Together, our findings demonstrate that phylogenomic synteny profiling across broad phylogenetic scales may provide valuable insights into genomic architecture, WGD history, and lineage-specific traits in organismal evolution.